Erschienen in: Standards in Genomic Sciences ; 5 (2011), 3. - S. 298-310

Standards in Genomic Sciences (2011) 5:298-310 DOI:10.4056/sigs.2215005

Complete genome sequence of lavamentivorans type strain (DS-1T)

David Schleheck1*, Michael Weiss1, Sam Pitluck2, David Bruce3, Miriam L. Land4, Shunsheng Han3, Elizabeth Saunders3, Roxanne Tapia3, Chris Detter3, Thomas Brettin4, James Han2, Tanja Woyke2, Lynne Goodwin3, Len Pennacchio2, Matt Nolan2, Alasdair M. Cook1, Staffan Kjelleberg5, Torsten Thomas5

1 Department of Biological Sciences and Research School Chemical Biology, University of Konstanz, Germany 2 DOE Joint Genome Institute, Walnut Creek, California, USA 3 Los Alamos National Laboratory, Bioscience Division, Los Alamos, New Mexico, USA 4 Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA 5 Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Science, University of New South Wales, Sydney, Australia

*Corresponding author: [email protected]

Keywords: Parvibaculum lavamentivorans DS-1, aerobic, Gram-negative, Rhodobiaceae, sur- factant biodegradation

Parvibaculum lavamentivorans DS-1T is the type of the novel genus Parvibaculum in the novel family Rhodobiaceae (formerly Phyllobacteriaceae) of the order Rhizobiales of Al- phaproteobacteria. Strain DS-1T is a non-pigmented, aerobic, heterotrophic bacterium and represents the first tier member of environmentally important bacterial communities that cata- lyze the complete degradation of synthetic laundry surfactants. Here we describe the features of this organism, together with the complete genome sequence and annotation. The 3,914,745 bp long genome with its predicted 3,654 protein coding genes is the first com- pleted genome sequence of the genus Parvibaculum, and the first genome sequence of a rep- resentative of the family Rhodobiaceae.

Introduction Parvibaculum lavamentivorans strain DS-1T P. lavamentivorans DS-1T is therefore an example (DSM13023 = NCIMB13966) was isolated for its of a first tier member of a two-step process that ability to degrade linear alkylbenzenesulfonate mineralizes environmentally important surfac- (LAS), a major laundry surfactant with a world- tants. wide use of 2.5 million tons per annum [1]. Strain Other representatives of the novel genus Parviba- DS-1T was difficult to isolate, is difficult to culti- culum have been recently isolated. Parvibaculum vate, and represents a novel genus in the Alpha- sp. strain JP-57 was isolated from seawater [6] [2,3]. Strain DS-1 catalyzes not only and is also difficult to cultivate [3]. Parvibaculum the degradation of LAS, but also of 16 other com- indicum sp. nov. was also isolated from seawater, mercially important anionic and non-ionic surfac- via an enrichment culture that degraded polycyc- tants (hence the species name lavamentivorans = lic aromatic hydrocarbons (PAH) and crude oil [7]. consuming [chemicals] used for washing [3]). The Another Parvibaculum sp. strain was isolated from initial degradation as catalyzed by strain DS-1T a PAH-degrading enrichment culture, using river involves the activation and shortening of the alkyl- sediment as inoculum [8]. Parvibaculum species chain of the surfactant molecules, and the excre- were also reported in a study on marine alkane- tion of short-chain degradation intermediates. degrading [9]. Parvibaculum species are These intermediates are then completely utilized frequently detected by cultivation-independent by other bacteria in the community [4,5]. methods, predominantly in habitats or settings

The Genomic Standards Consortium Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-177182 Schleheck et al. with hydrocarbon degradation. These include a succinate, or alkanes, alkanols and alkanoates (C8 - bacterial community on marine rocks polluted C16); no sugars tested were utilized [3]. with diesel oil [10], a bacterial community from To allow for growth in liquid culture with most of diesel-contaminated soil [11], a petroleum- the 16 different surfactants at high concentrations degrading bacterial community from seawater (e.g. for LAS, >1 mM; see [3].), the culture fluid [12], an oil-degrading cyanobacterial community needs to be supplemented with a solid surface, e.g. [13] and biofilm communities in pipes of a district polyester fleece or glass fibers [2,3]. The addition- heating system [14]. Parvibaculum species have al solid surface is believed to support biofilm for- also been detected in denitrifying, linear- mation, especially in the early growth phase when nonylphenol (NP) degrading enrichment cultures the surfactant concentration is high, and the or- from NP-polluted river sediment [15] and in ganism grows as single, suspended cells (non- groundwater that had been contaminated by li- motile) during the later growth phase. Growth near alkyl benzenes (LABs; non-sulfonated LAS] with a non-membrane toxic substrate (e.g. ace- [16]. Additionally, Parvibaculum species were tate) is independent of a solid surface, and consti- detected in biofilms that degraded polychlori- tutes suspended, single cells (motile). We presume nated biphenyls (PCBs) using pristine soil as in- that the biofilm formation by strain DS-1T is a pro- oculum [17], and in a PAH-degrading bacterial tective response to the exposure to membrane- community from deep-sea sediment of the West solubilizing agents (cf. [30]). Pacific [18]. Finally, Parvibaculum species were Based on the 16S rRNA gene sequence, strain DS1T detected in an autotrophic Fe(II)-oxidizing, ni- was described as the novel genus Parvibaculum, trate-reducing enrichment culture [19], as well as which was originally placed in the family Phyllo- in Tunisian geothermal springs [20]. The wide- bacteriaceae within the order Rhizobiales of Al- spread occurrence of Parvibaculum species in ha- phaproteobacteria [3,31]. The nearest well- bitats or settings related to hydrocarbon degrada- described organism to strain DS-1T is Afifella ma- tion implies an important function and role of rina (formerly marinum) (92% 16S these organisms in environmental biodegradation, rRNA gene sequence identity), a photosynthetic despite their attribute as being difficult to culti- purple, non-sulfur bacterium. The genus Rhodo- vate in a laboratory. bium was later re-classified as a member of the Here we present a summary classification and a novel family Rhodobiaceae [26,32], together with set of features for P. lavamentivorans DS-1T, to- two novel genera of other photosynthetic purple gether with the description of a complete genome non-sulfur bacteria (Afifella and ), sequence and annotation. The genome sequencing as well as with two novel genera of heterotrophic and analysis was part of the Microbial Genome aerobic bacteria, represented by the red- Program of the DOE Joint Genome Institute. pigmented baltica (gen. nov., sp. nov.) [33,34] and non-pigmented Tepidamorphus Classification and features gemmatus (gen. nov., sp. nov.) [35,36]. A phyloge- P. lavamentivorans DS-1T is a Gram-negative, non- netic tree (Figure 2) was constructed with the 16S pigmented, very small (approx. 1.0 × 0.2 µm), rRNA gene sequence of P. lavamentivorans DS-1T slightly curved rod-shaped bacterium that can be and that of (i) other isolated Parvibaculum strains, motile by means of a polar flagellum (Figure 1, (ii) representatives of other genera within the Table 1). Strain DS-1T grows very slowly on com- family Rhodobiaceae, (iii) representatives of the plex medium (e.g. on LB- or peptone-agar plates) genera in the family Phyllobacteriaceae, as well as, and forms pinpoint colonies only after more than (iv) representatives of other families within the two weeks of incubation. The organism can be order Rhizobiales. The phylogenetic tree shows quickly overgrown by other organisms. Larger now the placement of Parvibaculum species within colonies are obtained when the complex medium the family Rhodobiaceae, and that the Parvibacu- is supplemented with a surfactant, e.g. Tween 20 lum sequences clustered as a distinct evolutionary (see DSM-medium 884 [29]) or LAS [3]. When lineage within this family (Figure 2). This classifi- cultivated in liquid culture with mineral-salts me- cation of Parvibaculum has been adopted in the dium, strain DS-1T grows within one week with Ribosomal Database Project (RDP) and SILVA the single carbon sources acetate, ethanol, or rRNA Database Project, but not in the GreenGenes database. The family Rhodobiaceae has also not http://standardsingenomics.org 299 Parvibaculum lavamentivorans type strain (DS-1T) been included in the NCBI-, IMG- phosphatidyl glycerol, diphosphatidyl glycerol, taxonomy, and GOLD databases. phosphatidyl ethanolamine, phosphatidyl choline, Currently, 360 genome sequences of members of and two, unidentified aminolipids; the presence of the order Rhizobiales of have the two additional aminolipids appears to be dis- been made available (GOLD database; August tinctive of the organism [3]. The G+C content of 2011), and within the family Phyllobacteriaceae the DNA was determined to be 64% [3], which there are 21 genome sequences available corresponds well to the G+C content observed for (Chelativorans sp. BNC1, Hoeflea phototrophica the complete genome sequence (see below). DFL-43, and 18 Mesorhizobium strains). No ge- nome sequences currently exist for a representa- Genome sequencing information tive of the novel family Rhodobiaceae, except of Genome project history the genome of P. lavamentivorans DS-1T. The genome was selected for sequencing as part of the U.S. Department of Energy - Microbial Ge- Chemotaxonomy nome Program 2006. The DNA sample was sub- Examination of the respiratory lipoquinone com- mitted in April 2006 and the initial sequencing position of strain DS-1T showed that ubiquinones phase was completed in October 2006. The ge- are the sole respiratory quinones present, and the nome finishing and assembly phase were com- major lipoquinone is ubiquinone 11 (Q11) [3]. The pleted in June 2007, and presented for public fatty acids of P. lavamentivorans are straight chain access on December 2007; a modified version was saturated and unsaturated, as well as ester- and presented in February 2011. Table 2 presents the amide-linked hydroxy-fatty acids, in membrane project information and its association with MIGS fractions [3]. The major polar lipids are version 2.0 compliance [39].

Figure 1. Scanning electron micrograph of P. lavamentivorans DS-1T. Cells derived from a liquid culture that grew in acetate/mineral salts medium. 300 Standards in Genomic Sciences Schleheck et al.

Figure 2. Phylogenetic tree of 16S rRNA gene sequences showing the position of P. lavamentivorans DS-1T relative to other type strains within the families Rhodobiaceae, Phyllobacteriaceae and other families in the order Rhizo- biales (see the text). Strains within the Rhodobiaceae and Phyllobacteriaceae shown in bold have genome projects underway or completed. The corresponding 16S rRNA gene accession numbers (or draft genome sequence iden- tifiers) are indicated. The sequences were aligned using the GreenGenes NAST alignment tool [37]; neighbor- joining tree building and visualization involved the CLUSTAL and DENDROSCOPE software [38]. Caulobacterales sequences were used as outgroup. Bootstrap values >30 % are indicated; bar, 0.01 substitutions per nucleotide po- sition.

http://standardsingenomics.org 301 Parvibaculum lavamentivorans type strain (DS-1T) Table 1. Classification and general features of Parvibaculum lavamentivorans DS-1T. MIGS ID Property Term Evidence codea Domain Bacteria TAS [21] Phylum Proteobacteria TAS [22] Class Alphaproteobacteria TAS [23,24] Current classification Order Rhizobiales TAS [23,25] Family Rhodobiaceae TAS [23,26] Genus Parvibaculum TAS [3] Species Parvibaculum lavamentivorans TAS [3] Type strain DS-1 Gram stain negative TAS [3] Cell shape small rod TAS [3] Motility motile TAS [3] Sporulation non-sporulating TAS [3] Temperature range mesophile TAS [3] Optimum temperature 30 ºC TAS [3]

Carbon source acetate, ethanol, pyruvate, succinate, alkanes (C8 – TAS [2,3,5,7]

C16), various anionic and non-ionic surfactants Energy source chemoorganotroph TAS [3] Terminal electron receptor molecular oxygen TAS [3] MIGS-6 Habitat aerobic habitat TAS [2,27] MIGS-6.3 Salinity 0 – 3% NaCl TAS [3] MIGS-22 Oxygen requirement aerobic TAS [3] MIGS-15 Biotic relationship free-living TAS [3] MIGS-14 Pathogenicity none TAS [3]

isolated from a surfactant-degrading laboratory trick- ling filter that was inoculated with sludge of an indus- MIGS-4 Geographic location TAS [2] trial sewage treatment plant in Ludwigshafen, Germany

MIGS-5 Sample collection time 1999 TAS [2] MIGS-4.1 Latitude 49.48 TAS [2] MIGS-4.2 Longitude 8.44 TAS [2] MIGS-4.3 Depth MIGS-4.4 Altitude 96 m TAS [2] a) Evidence codes - IDA: Inferred from Direct Assay; TAS: Traceable Author Statement (i.e., a direct report exists in the literature); NAS: Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence). These evidence codes are from of the Gene Ontology project [28].

302 Standards in Genomic Sciences Schleheck et al. Table 2. Project information MIGS ID Property Term MIGS-31 Finishing quality Finished MIGS-28 Libraries used 3.5 kb, 9 kb and 37 kb DNA libraries MIGS-29 Sequencing platforms Sanger MIGS-31.2 Sequence coverage 16× MIGS-30 Assemblers Phred/Phrap/Consed MIGS-32 Gene calling method Glimmer/Criteria Genbank ID 17639 Genbank Date of Release July 31, 2007 GOLD ID Gc00631 MIGS-13 Source material identifier DSM 13023 = NCIMB 13966 Project relevance Biodegradation, biotechnological

Growth conditions and DNA isolation P. lavamentivorans DS-1T was grown on LB agar The completed genome assembly contains plates (2 weeks) and pinpoint colonies were 76,885 reads, achieving an average of 16-fold transferred into selective medium (1 mM sequence coverage per base with an error rate LAS/minimal salts medium; with glass-fiber sup- less than 5 in 100,000. plement, 5-ml scale [3]). This culture was sub- cultivated to larger scale (100-ml and 1-liter Genome annotation scale) in 30 mM acetate/minimal salts medium; Genes were identified using a combination of cell pellets were stored frozen until DNA prepara- Critica [47] and Glimmer [48] as part of the ge- tion. DNA was prepared following the JGI DNA nome annotation pipeline at Oak Ridge National Isolation Bacterial CTAB Protocol [40]. Laboratory (ORNL), Oak Ridge, TN, USA, followed by a round of manual curation. The predicted Genome sequencing and assembly CDSs were translated and used to search the Na- The genome of P. lavamentivorans DS-1T was se- tional Center for Biotechnology Information quenced at the Joint Genome Institute (JGI) using (NCBI) non-redundant database, UniProt, TIGR- a combination of 3.5 kb, 9 kb and 37 kb DNA li- Fam, Pfam, PRIAM, KEGG, COG, and InterPro da- braries. All general aspects of library construc- tabases; miscellaneous features were predicted tion and sequencing performed at the JGI can be using TMHMM [49] and signalP [50]. These data found at the JGI website [41]. Draft assemblies sources were combined to assert a product de- were based on 76,870 reads. Combined, the reads scription for each predicted protein. The tRNAS- from all three libraries provided 16-fold coverage canSE tool [51] was used to find tRNA genes, of the genome. The Phred/Phrap/Consed soft- whereas ribosomal RNAs were found by using ware package [42] was used for sequence assem- BLASTn against the ribosomal RNA databases. bly and quality assessment [43-45]. After the The RNA components of the protein secretion shotgun stage, reads were assembled with paral- complex and the RNaseP were identified by lel phrap (High Performance Software, LLC). searching the genome for the corresponding Possible mis-assemblies were corrected with Rfam profiles using INFERNAL [52]. Additional Dupfinisher [46], PCR amplification, or transpo- gene prediction analysis and manual functional son bombing of bridging clones (Epicentre Bio- annotation was performed within the Integrated technologies, Madison, WI, USA). Gaps between Microbial Genomes (IMG) platform [41] devel- contigs were closed by editing in Consed, custom oped by the Joint Genome Institute, Walnut primer walk or PCR amplification (Roche Applied Creek, CA, USA [53]. Science, Indianapolis, IN, USA). A total of 24 pri- mer walk reactions were necessary to close gaps and to raise the quality of the finished sequence. http://standardsingenomics.org 303 Parvibaculum lavamentivorans type strain (DS-1T) Genome properties amino acids and essential co-factors, and the cen- The genome of P. lavamentivorans DS-1T compris- tral metabolism is represented by a complete es one circular chromosome of 3,914,745 bp pathway for the citrate cycle, glycoly- (62.33% GC content) (Figure 3), for which a total sis/gluconeogenesis, and the non-oxidative number of 3,714 genes were predicted. Of these branch of the pentose-phosphate pathway; no predicted genes, 3,654 are protein-coding genes, candidate genes for the oxidative branch of the and 2,723 of the protein-coding genes were as- pentose-phosphate pathway or for the Entner– signed to a putative function and the remaining Doudoroff pathway are predicted. annotated as hypothetical proteins; 18 pseudo- P. lavamentivorans DS-1T does not grow on D- genes were also identified. A total of 60 RNA genes glucose, D-fructose, maltose, D-mannitol, D- and one rRNA operon are predicted; the latter is mannose, and N-acetylglucosamine [3,7], and reflective of the slow growth of P. lavamentivorans there are no valid candidate genes predicted in the DS-1T [54,55]. Furthermore, one Clustered Regu- genome for ATP-dependent sugar uptake systems larly Interspaced Short Palindromic Repeats ele- or for D-glucose uptake via a phosphotransferase ment (CRISPR) including associated protein genes system. Similarly, no valid candidate genes were were predicted. The properties and the statistics predicted for ATP-dependent amino-acid and of the genome are summarized in Table 3, and the di/oligo-peptide transport systems or for other distribution of genes into COGs functional catego- amino-acid/peptide transporters, which reflects ries is presented in Table 4. the poor growth of strain DS-1T in complex me- dium (LB-medium). Metabolic features The genome of P. lavamentivorans encodes com- plete pathways for synthesis of all proteinogenic

Table 3. Nucleotide and gene count levels of the genome of P. lavamentivorans DS-1T Attribute Value % of totala Genome size (bp) 3,914,745 100 DNA coding region (bp) 3,535,064 90.30 G+C content (bp) 2,439,986 62.33 Number of replicons 1 Extrachromosomal elements 0 Total genes 3,714 100 RNA genes 60 1.62 rRNA operons 1 Protein-coding genes 3,654 98.38 Pseudo genes 18 0.48 Genes with function prediction 2,723 73.32 Genes in paralog clusters 620 16.69 Genes assigned to COGs 2,904 78.19 Genes assigned to Pfam domains 3,054 82.23 Genes with signal peptides 717 19.31 Genes connected to KEGG pathways 1,085 29.21 Genes with transporter classification 430 11.58 Genes with transmembrane helices 782 21.06 CRISPR count 1 % of totala a) The total is based on either the size of the genome in base pairs or the total number of protein coding genes in the annotated genome.

304 Standards in Genomic Sciences Schleheck et al. Table 4. Number of genes associated with the general COG functional categories in P. lavamentivorans DS-1T Code Value %age Description J 163 5.07 Translation, ribosomal structure and biogenesis A 1 0.0 RNA processing and modification K 243 7.0 Transcription L 137 3.9 Replication, recombination and repair B 1 0.0 Chromatin structure and dynamics D 25 0.7 Cell cycle control, mitosis and meiosis Y 0 0.0 Nuclear structure Z 0 0 Cytoskeleton W 0 0 Extracellular structures V 85 2.4 Defense mechanisms T 118 3.4 Signal transduction mechanisms M 131 3.8 Cell wall/membrane biogenesis N 6 0.2 Cell motility U 39 1.1 Intracellular trafficking and secretion O 77 2.2 Posttranslational modification, protein turnover, chaperones C 153 4.4 Energy production and conversion G 294 8.4 Carbohydrate transport and metabolism E 214 6.1 Amino acid transport and metabolism F 79 2.3 Nucleotide transport and metabolism H 110 3.2 Coenzyme transport and metabolism I 73 2.1 Lipid transport and metabolism P 152 4.4 Inorganic ion transport and metabolism Q 30 0.9 Secondary metabolites biosynthesis, transport and catabolism R 318 9.1 General function prediction only S 200 5.7 Function unknown - 1082 31.0 Not in COGs

For the assimilation of acetyl-CoA from the degra- oxygenation to activate the chain) supplemented dation of alkanes and surfactants [2,3,5], or during by a variety of genes predicted for omega- growth with acetate, the genome of P. lavamenti- oxidations (to generate the corresponding fatty- vorans encodes the glyoxylate cycle (isocitrate acids) and fatty-acid beta-oxidations (to excise lyase, Plav_0592; malate synthase, Plav_0593) to acetyl-CoA units). We are currently exploring this generate succinate for the synthesis of carbohy- high abundance of genes for alkane/alkyl- drates. The genome also encodes the complete utilization in strain DS-1T by transcriptional and ethyl-malonyl-CoA pathway to assimilate acetate translational analysis [unpublished]. For example, [56]. This observation, i.e. glyoxylate cycle and at least nine cytochrome-P450 (CYP) alkane mo- ethyl-malonyl-CoA pathway in the same organism, nooxygenase (COG2124), 44 alcohol dehydroge- has been made before [57], and these two path- nase (COG1028), 11 aldehyde dehydrogenase ways in P. lavamentivorans DS-1T might be diffe- (COG1012), 20 acyl-CoA synthetase (COG0318), rentially expressed under varying environmental 40 acyl-CoA dehydrogenase (COG1960), 31 enoyl- conditions. CoA hydratase (COG1024), 14 acyl-CoA acetyl- For the degradation of alkanes and surfactants transferase (COG0183), six thioesterase through abstraction of acetyl-CoA [54], the ge- (COG0824), and 17 putative long-chain acyl-CoA nome contains a wealth of candidate genes for the thioester hydrolase (PF03061) candidate genes entry into alkyl-chain degradation (omega- are predicted in the genome. http://standardsingenomics.org 305 Parvibaculum lavamentivorans type strain (DS-1T)

Figure 3. Graphical circular map of the genome of P. lavamentivorans DS-1T. From outside to center: Genes on forward strand (color by COG categories), genes on reverse strand (color by COG categories), RNA genes (tRNA, green; rRNA, red; other RNAs, black), GC content, GC skew.

Other predicted oxygenase genes comprise three in the degradation pathway [60]) and geraniol, putative Baeyer-Villiger-type FAD-binding mo- citronellol, linalool, menthol and eucalyptol (for nooxygenase genes (COG2072). Cyclohexanone the involvement of acyl-CoA interconversion en- and hydroxyacetophenone, which are putative zymes in the degradation pathways) as substrates substrates for such oxygenases (e.g [58,59]) were for growth were also tested negative. tested as carbon source for growth of strain DS-1T, In contrast to the high abundance of genes for ali- as well as cycloalkanes (C6, C8, C12), however, none phatic-hydrocarbon degradation, the genome con- supported growth. The terpenoids camphor (for tains few genes for aromatic-hydrocarbon degrada- the involvement of a cytochrome-P450 oxygenase tion. One gene set for an aromatic-ring dioxygenase

306 Standards in Genomic Sciences Schleheck et al. component (Plav_1761 and 1762; BenAB-type), phenyl-propionate, or phenylalanine and tyrosine as three aromatic-ring monooxygenase component carbon source when tested. genes (Plav_1541 and 0131, MhpA-type; Plav_1785, Finally, P. lavamentivorans DS-1T is predicted to HpaB-type), and three valid candidate genes for store carbon in form of intracellular polyhydroxy- extradiol ring-cleavage dioxygenase (Plav_1539 [61] alkanoate/butyrate (PHB) as its genome encodes and 1787, BphC-type; Plav_0983, LigB-type) were a PHB-synthase (PhbC) gene (Plav_1129), PHB- predicted in the genome. Strain DS-1T did not grow depolymerase (PhaZ) gene (Plav_0012), and PHB- with benzoate, protocatechuate, phenylacetate, synthesis repressor (PhaR) gene (Plav_1572).

Acknowledgements We thank Joachim Hentschel for SEM operation. The Science of the U.S. Department of Energy under Con- work was supported by the University of Konstanz and tract No. DE-AC02-05CH11231, and that of the Univer- the Konstanz Research School Chemical Biology, the sity of California, Lawrence Livermore National Labora- University of New South Wales and the Centre for Ma- tory under Contract No. W-7405-Eng-48, Lawrence rine Bio-Innovation, and the Deutsche Forschungsge- Berkeley National Laboratory under contract No. DE- meinschaft (DFG grant SCHL 1936/1-1 to D.S.). The AC03-76SF00098, and Los Alamos National Laboratory work conducted by the U.S. Department of Energy Joint under contract No. W-7405-ENG-36. Genome Institute was supported by the Office of

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